Default mode network alterations in individuals with high-trait-anxiety: An EEG functional connectivity study

Highlights

• The association between trait anxiety and EEG DMN connectivity was investigated.

• High-trait-anxiety individuals showed a decrease of theta and beta connectivity.

• DMN connectivity strength was negatively related with STAI-T total score.

• Our results suggest that high-trait-anxiety individuals fail to synchronize DMN.

Abstract

Background

Although several researches investigated Default Mode Network (DMN) alterations in individuals with anxiety disorders, up to now no studies have investigated DMN functional connectivity in non-clinical individuals with high-trait-anxiety using quantitative electroencephalography (EEG). Here, the main aim was to extend previous findings investigating the association between trait anxiety and DMN EEG functional connectivity.

Methods

Twenty-three individuals with high-trait-anxiety and twenty-four controls were enrolled. EEG was recorded during 5 min of resting state (RS). EEG analyses were conducted by means of the exact Low-Resolution Electromagnetic Tomography software (eLORETA).

Results

Compared to controls, individuals with high-trait-anxiety showed a decrease of theta connectivity between right medial prefrontal cortex (mPFC) and right posterior cingulate/retrosplenial cortex. A decrease of beta connectivity was also observed between right mPFC and right anterior cingulate cortex. Furthermore, DMN functional connectivity strength was negatively related with STAI-T total score (i.e., lower connectivity was associated with higher trait anxiety), even when controlling for potential confounding variables (i.e., sex, age, and general psychopathology).

Limitations

Small sample size makes it difficult to draw definitive conclusions. Furthermore, we did not assess state variation of anxiety, which make our interpretation specific to trait anxiety.

Conclusions

Taken together, our results suggest that high-trait-anxiety individuals fail to synchronize DMN during RS, reflecting a possible top-down cognitive control deficit. These results may help in the understanding of the individual differences in functional brain networks associated with trait anxiety, a crucial aim in the prevention and in the early etiology understanding of clinical anxiety and related sequelae.

Introduction

“Trait anxiety” refers to a relatively stable individual difference characterized by harm avoidance behavior (e.g., worrying), difficulty to relax and tendency to perceive a wide range of environmental events as dangerous and threatening (Spielberger and Sydeman, 1994, Sylvers et al., 2011). High anxiety trait is considered a crucial vulnerability factor for psychopathology, especially for mood and anxiety disorders (Weger and Sandi, 2018).

From a neurophysiological and neurobiological point of view, several studies have shown that individuals with high-trait-anxiety are characterized by different brain structural and functional alterations (Sylvers et al., 2011). For example, it has been reported that high trait anxiety is associated with reduced thickness in the medial prefrontal cortex (mPFC) (Hu and Dolcos, 2017, Kuhn et al., 2011, Spampinato et al., 2009), precuneus (Miskovich et al., 2016) and restrosplenial cortex (Spampinato et al., 2009). Furthermore, functional magnetic resonance imaging (fMRI) investigations in individuals with high-trait-anxiety revealed abnormal activations of both cortical (e.g., PFC) and subcortical regions (e.g., amygdala) during emotional (Comte et al., 2015, Dickie and Armony, 2008, Etkin et al., 2004, Stein et al., 2007) and cognitive tasks (Basten et al., 2011, Basten et al., 2012, Bishop, 2009, Zhang et al., 2016) as well as during resting state (RS) condition (Baur et al., 2013, Kim et al., 2011, Modi et al., 2015, Tian et al., 2016, Yin et al., 2016). Finally, quantitative electroencephalographic (qEEG) studies (i.e., EEG coherence and EEG power spectra) showed that high trait anxiety is associated with several neurophysiological abnormalities, such as increased cortical arousals and EEG desynchronization, during emotional stimuli processing (Aftanas et al., 1996, Aftanas and Pavlov, 2005, Aftanas et al., 2003, Knyazev et al., 2008), anxiogenic situations (Knyazev et al., 2005, Knyazev et al., 2006b), cognitive tasks (Knyazev et al., 2006a, Savostyanov et al., 2009) and RS condition (Aftanas and Pavlov, 2005, Knyazev et al., 2004, Pavlenko et al., 2009, Putman, 2011).

An important advance in neuroscience research, reflecting the modern concept of the brain as a highly integrated and dynamic system, is the assessment of functional connectivity in brain networks (i.e., a set of areas with activity that tends to increase or decrease in synchrony), in both healthy and neuropsychiatric patients (Sylvester et al., 2012).

The Default Mode Network (DMN) is one of the functional brain networks that most frequently shows abnormalities associated with psychopathology (Broyd et al., 2009, Whitfield-Gabrieli and Ford, 2012). It is thought to be involved in several higher-order integrative mental functions, including self-consciousness, self-processing and emotion regulation (Schilbach et al., 2008, Sylvester et al., 2012). The DMN is predominantly detected during the RS condition, when individuals are not actively engaged in goal-directed or attention-demanding tasks (Cicerale et al., 2013, Mak et al., 2017, Neuner et al., 2014). It has been conceptualized as a distributed network characterized by high neural activity and temporal synchrony among different brain regions, such as anterior cingulate cortex (ACC), posterior cingulate/retrosplenial cortex (PCC/Rsp), mPFC, temporoparietal junction (TPJ) (Buckner et al., 2008, Mak et al., 2017, Thatcher et al., 2014, Whitfield-Gabrieli and Ford, 2012).

Although several researches investigated DMN alterations in patients with anxiety disorders (Kim and Yoon, 2018, Peterson et al., 2014), up to now, only few studies selectively focused on non-clinical individuals with high trait anxiety. Modi et al. (2015), in a fMRI study, reported that, compared to individuals with low-trait-anxiety, participants with high-trait-anxiety showed reduced functional connectivity in several regions of the DMN, such as right PCC, left temporal and parietal lobe. Similarly, more recently, Zidda et al. (2018) documented that connectivity strength of right amygdala and hippocampus with the DMN were negatively related to trait anxiety (i.e., individuals with high-trait-anxiety show reduced connectivity).

To the best of our knowledge, no studies have investigated DMN functional connectivity in individuals with high-trait-anxiety using qEEG, a suitable tool for the assessment of this network (Neuner et al., 2014, Thatcher et al., 2014) offering an important source of information for researchers and clinicians (e.g. qEEG data directly relate to dynamic postsynaptic activity in the cerebral cortex with a high temporal resolution) (Canuet et al., 2011). Therefore, the main aim of the present study was to extend these previous findings investigating the association between trait anxiety and DMN EEG functional connectivity, using the exact Low Resolution Electromagnetic Tomography software (eLORETA), a validated tool for localizing sources of brain electric activity (Pascual-Marqui et al., 1994).